Learning to breathe and sing: development of respiratory-vocal coordination in young songbirds

How do animals with learned vocalizations coordinate vocal production with respiration? Songbirds such as the zebra finch learn their songs, beginning with highly variable babbling vocalizations known as subsong. After several weeks of practice, zebra finches are able to produce a precisely timed pattern of syllables and silences, precisely coordinated with expiratory and inspiratory pulses (Franz M, Goller F. J Neurobiol 51: 129-141, 2002). While respiration in adult song is well described, relatively little is known about respiratory patterns in subsong or about the processes by which respiratory and vocal patterns become coordinated. To address these questions, we recorded thoracic air sac pressure in juvenile zebra finches prior to the appearance of any consistent temporal or acoustic structure in their songs. We found that subsong contains brief inspiratory pulses (50 ms) alternating with longer pulses of sustained expiratory pressure (50-500 ms). In striking contrast to adult song, expiratory pulses often contained multiple (0-8) variably timed syllables separated by expiratory gaps and were only partially vocalized. During development, expiratory pulses became shorter and more stereotyped in duration with shorter and fewer nonvocalized parts. These developmental changes eventually resulted in the production of a single syllable per expiratory pulse and a single inspiratory pulse filling each gap, forming a coordinated sequence similar to that of adult song. To examine the role of forebrain song-control nuclei in the development of respiratory patterns, we performed pressure recordings before and after lesions of nucleus HVC (proper name) and found that this manipulation reverses the developmental trends in measures of the respiratory pattern.